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Epidemiology International Journal Research Article 18 min read

Influence of Environmental Factors on Occurrence of Leptospirosis in Humans and Animals in Brazil-A Review

Marchi MNA*
* Corresponding author
ISSN: 2639-2038  10.23880/eij-16000241  Received: July 15, 2022  Published: July 28, 2022
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Keywords
One Health Risk factors Zoonosis Public Health Epidemiology
Abstract

Leptospirosis is an infectious, zoonotic and neglected disease, distributed worldwide and endemic in America and in several states of Brazil. It is a disease that causes significant social, economic and health impact. Pathogenic species can survive in the environment for relatively long periods. Some environmental conditions favor the survival and maintenance of the bacteria in the environment, such as characteristics of the soil to be alkaline and humid, type of agricultural production and proximity to farm Animals. Animals play an important role in environmental contamination, especially rodents. The findings in this review reinforce the need for an integrated approach from a one health perspective so that prevention actions are more effective.

Introduction

Leptospirosis is an infectious, zoonotic and neglected disease, distributed worldwide and endemic in America and in several states of Brazil [1]. The etiological agent of this disease is a bacterium of the genus Leptospitospira, which has as reservoir several animal species, and the environment is fundamental for the analysis of risk factors in a multidisciplinary approach, as in single [1, 2, 3]. In America, out of 52 countries and territories, 28 reported the presence of human cases. A total of 10.433 human cases of leptospirosis were reported in the Region of the Americas. The regional cumulative incidence rate was of 2.11 per 100,000 inhabitants. Brazil reported 38% of human cases in the Region of the Americas in the same period [4]. However, leptospirosis remains a silent disease, mainly due to the scarcity of data in many countries [5].

The diversity of reservoir animals represents a significant challenge for prevention and control [6], and synanthropic rodents and dogs play the role of the main reservoirs of the disease. Exposure to water and soil contaminated by the urine of infected animals is the most common route of transmission of people and domestic animals [7]. In addition, geological and geographic characteristics together with demographic, agricultural and livestock factors are also determinant for transmission [8]. Understanding the factors that influence the strong occurrence of leptospirosis in Brazil is essential for the elaboration of public policies directed to the control and prevention of the disease [8]. It is also important to extrapolate the understanding of these factors in other territories of the world. Thus, this study aims to understand the influence of environmental factors in the occurrence of leptospirosis in humans in Brazil through a literature review.

Social Impacts of Leptospirosis

Leptospirosis is a zoonosis of worldwide distribution, caused by bacteria of the genus Leptospira. The disease may present with nonspecific signs such as fever, myalgia, abdominal pain, vomiting, and evolving to hematuria and petechiae. Some patients develop the most severe form of the disease, known as Weil syndrome, in which the patient may have intravascular hemolysis, hemorrhagic manifestations, renal and hepatic involvement [9]. Infected animals may be asymptomatic, capable of releasing Leptospiras for months, years or throughout life continuously and intermittently, depending on the serovar involved and the species of the infected animal [10]. Worldwide, around 1.3 million and 300,000 cases of leptospirosis are recorded in humans, with incidence rates ranging from 0.1 to 975.0 cases per 100,000 inhabitants [11]. In Brazil, the highest incidence per 100,000 inhabitants was observed in the southern region, in 2011 (4.46), followed by the North (2.27), Southeast (1.73), Northeast (1.34) and Midwest (0.39) regions [12].

It is a disease that causes significant social, economic and health impact. According to the Ministry of Health (MS), the disease has great social and economic importance due high incidence and significant percentage of hospitalizations, high hospital costs and loss of working days, as well as its lethality [2]. Pereira C [13] concluded that 3,492 cases of leptospirosis occurred in 2008 generated an approximate cost of R$ 1,542,526 and 10,664 potential years of life lost to the Brazilian health system. In addition, the sick people presented loss of productivity, which ranged between R$ 278,481.60 to R$ 979,317. After a partial economic evaluation of the cost-illness type from the economic and social perspective, authors pointed out that the disease produces a financial impact on society due to the high number of potential years of life lost and salaries that are not received by the patient [2]. Similarly, in this other study, the authors identify that, in 2007, the age group that lost the most years of life, belonged to the group of 20 to 49 years, a phase of life of high creativity and productivity [2].

In humans, leptospirosis has been related to a low level of education [2]. The sociodemographic profile of individuals with leptospirosis coincides with the incidence in poor areas, poor sanitation, in addition to regions where flooding occurs [11, 14]. The presence of rodents in areas with these characteristics has been described previously and is the main factor associated with [15]. In several studies the higher prevalence of affected individuals is male [14, 16]. This is due to the fact that men are at the forefront of activities involving risk situations [14], such as animal management, agricultural work, maintenance of sewage network, among other occupations [17].

Pathogenic Species in the Environment

Transmission of leptospirosis can occur through the direct route; which occurs through the host’s contact with blood, urine, or other reservoir fluid, which contains leptospiras; and the indirect route, in which contact with leptospiras occurs through contaminated soil or water [18, 19]. The indirect route highlights the importance of studies of environmental factors, for a better understanding of this link of transmission [20, 21].

Leptospires are mobile bacteria, 6 to 20 μm long and helically coiled. They are spirochetes belonging to the family Leptospiraceae [22]. The genus Leptospira is traditionally divided into two groups, the saprophytes, Leptospira biflexa sensu lato, and the pathogenic, Leptospira interrogans sensu lato. After a phylogenetic analysis, it was revealed that leptospira can be divided into three strains correlated with the pathogenicity level of the species: saprophyte, intermediate and pathogenic [23]. Intermediate species share an almost common ancestor with pathogenic species, exhibiting moderate pathogenicity in humans and animals. Different serovars of leptospira have been isolated from environmental sources as they are able to survive in humid soil and fresh water for several weeks [24, 25]. Leptospira’s ability to occupy several ecological niches is undoubtedly due to a diversity of mechanisms, such as signal transduction systems encoded by its large genome and that allow it to adapt and resist adverse conditions [26, 27].

The discovery of new species of leptospira, including species belonging to the pathogen and intermediate strains is fundamental for the development of robust detection and diagnostic tools that are necessary to treat infected hosts more quickly and appropriately. The characterization of leptospira populations in soil and water is also important for prevention and control actions aimed at reducing the risk of infection by bacteria in the environment [28]. Thus, recent studies have isolated new species of leptospira in the soil [29, 30], leading to an important expansion of taxonomy, with currently 35 species named [30, 31]. It is believed that virulent pathogenic leptospiras cannot multiply in the environment [32]. However, although the survivability of most species outside a host is not questionable, little is known about the environmental factors and determinants that condition this survival [33]. Leptospira’s ability to adapt to parameters such as osmolarity within a host or in nature also showed to be species-specific and related to genome size [34].

Viability of Bacteria in the Environment

Knowledge about the biology and survival mechanisms of pathogenic leptospiras in the environment is still scarce, and the ability of different strains to survive in environmental conditions remains largely unexplored. However, the understanding of these factors is of paramount importance for a better understanding of the epidemiology of the disease and a better control and prevention of human leptospirosis [35].

Recognizing this importance, some studies to evaluate the viability of leptospira in environment have been conducted. Although the real-time PCR technique detects leptospiras in environmental samples, it does not provide information regarding the viability of these cells. For this, studies have combined PCR methods with the use of propidium monoazide to reduce the detection of dead or membrane-compromised cells. This technique, known as PCR-feasibility, provides leptospira’s viability indications in environmental samples [25, 36]. Recently, some researchers have optimized procedures for the molecular detection of pathogenic leptospiras from environmental water sources [37], increasing the possibilities of further studies on environmental leptospirosis and opening up pathways for one health studies of this complex zoonosis [35].

Saprophyte species, common inhabitants of the environment, are abundant and grow faster, are the most often isolated from soil and water samples [38, 39]. But pathogenic species such as L. interrogans have already been detected in surface waters and from rice planting [40]. In a systematic review, strong evidence was found that virulent pathogenic leptospiras may remain viable and have the potential to infect people and/or animals in the environment for months, especially in soils [35]. In addition, they were isolated more frequently in the soil than in standing waters, currents or springs [35, 41, 42].

Associated Environmental Factors

Not only is leptospirosis a public health issue in developing countries, like Brasil, it has become an urban health problem in developed and industrialized countries, especially during periods of seasonal reinfall and flooding in unsanitary environments. The disease is also occurring in countries that natural disasters like hurricanes, typhoons and floods, is relatively common [15]. In urban areas in Brazil, especially in poor conditions of basic sanitation and paving, such as slums in large centers, associated with floods, soil contamination is a relevant risk factor for the population. In this setting, it is described that contact with the remaining mud of floods has a strong association with the occurrence of the disease in humans when compared to people’s contact with the water itself [43].

Some environmental components have been related to the occurrence of the disease, including soil type and use, as well as vegetation cover and predominant climate. It is suspected that alkaline and neutral soil promotes a longer survival of the bacterium, especially in young and unstructured soils, such as those of volcanic origin [44]. Added to these, soil temperature and proximity to water bodies have also been reported as potential facilitators for bacterial survival [41]. In addition, the incidence of leptospirosis is seasonal, usually peaking in summer and autumn, in temperate climate countries and during the rainy seasons in tropical climates [45]. Lower altitudes are associated with the higher occurrence of leptospirosis. They are places with a greater propensity for flooding. Low altitudes also usually have higher temperatures and this type of environment have favored the maintenance of the bacteria [8, 46]. Rainfall is another important factor for maintaining moisture [47].

Leptospirosis is endemic in rural and urban regions [48]. In southern Brazil, the rural population has an eight-fold higher risk of acquiring the disease compared to the urban population. In addition, the largest number of cases in these areas is concentrated in places where tobacco and rice are cultivated, due to the characteristic of Schneider MC, et al. [49]. Other types of production, such as grains, have their harvest and storage, attractive factors for rodents, favoring environmental contamination [50, 51]. Brazil is a major grain producer, and this may be a risk factor for rural populations [47]. Spatial analysis studies have shown the association of leptospirosis with the territory. They have also associated the disease with various aspects and characteristics belonging to the studied environment [8, 47, 52].

Farm Animals and the Environment

In addition to rodents, domestic animals have participated in the epidemiological chain of leptospirosis, because they act as carriers and potential transmitters of the disease [17]. Dogs, serovar maintenance hosts Canicola, but which can also bear other serovars such as Pyrogenes, Castellonis, Autumnalis, Icterohaemorrhagiae [53, 54, 55, 56, 57], live close to humans, especially in urban areas. Animais de produção também possuem participação na manutenção da leptospira no ambiente. Recentemente, 17 sorovares da bactéria foram encontrados em bovinos, equinos, ovinos e suínos, sendo que as mais frequentes foram Celledoni, e Icteroheamorrhagiae e sorogrupo Serjoe. As suas últimas também foram encontradas em humanos na mesma região [50]. Em bovinos, a soroprevalência é relativamente alta no sul do Brasil (44,69%) e os fatores de risco mais relevantes são a baixa altitude e a elevada temperatura [58]. Alguns fatores de risco para a doença em suínos é a presença de bebedouros do tipo canaleta, a presença de áreas alagadiças próximas às instalações dos animais e a falta de higienização dos reservatórios de água [59].

Embora as espécies animais mencionadas possam ter participação na contaminação ambiental, o principal transmissor de leptospiras patogênicas são os ratos. Desses, o R.  norvegicus e R.  rattus, apresentam a maior prevalência de leptospira em diversas partes do mundo [15], sendo o R. novergicus, o hospedeiro definitivo do sorovar Icterohaemorrhagiae, o mais patogênico ao homem [60]. Leptospirosis is an excellent example of one health, as it is a disease that integrates human medicine, veterinary medicine and environmental health, due to the diversity of species and serovars, hosts and conditions of survival in the environment [50]. Thus, the one health approach is essential for the development of control and prevention measures, which need to be multidisciplinary and multisectoral [3].

Conclusion

Leptospirosis is a disease of wide distribution in Brazil that has social and economic impacts. The survival of pathogenic strains in the environment depends on soil conditions and their use. Alkaline soils with fewer nutrients favor the maintenance of the bacterium in the environment. The disease occurs more in rural areas in some regions of Brazil, when the conditions of some plantations such as rice, tobacco and grains are attractive to rodents, in addition to the greater proximity of humans to other susceptible animals. In urban areas, the occurrence of leptospirosis is associated with large centers, floods and precarious basic sanitation, associated with the presence of mud, more than the water itself. Those exposed in this review reinforce the importance of an integrated approach to the prevention of leptospirosis in humans.

References

  1. Schneider MC, Leonel DG, Hamrick PN, de Caldas EP, Velásquez RT, et al. (2017) Leptospirosis in Latin America: exploring the first set of regional data Original research. Pan Am J Public Heal 41: e81.
  2. Souza VMM, Arsky MLNS, Castro APB, Araujo WN (2011) Anos potenciais de vida perdidos e custos hospitalares da leptospirose no Brasil. Rev Saude Publica 45(6): 1001-1008.
  3. King LJ, Anderson LR, Blackmore CG, Blackwell MJ, Lautner EA, et al. (2008) Executive summary of the AVMA One Health Initiative Task Force report. J Am Vet Med Assoc 233(2): 259-261.
  4. (2015) Leptospirosis: Region of the Americas. PAHO.
  5. Schneider M, Jancloes M, Buss D, Aldighieri S, Bertherat E, et al. (2013) Leptospirosis: A Silent Epidemic Disease. Int J Environ Res Public Health 10(12): 7229-7234.
  6. Petrakovsky J, Bianchi A, Fisun H, Aguilar PN, Pereira MM (2014) Animal Leptospirosis in Latin America and the Caribbean Countries: Reported Outbreaks and Literature Review (2002-2014). Int J Environ Res Public Health 11(10): 10770-10789.
  7. (2003) Human leptospirosis : guidance for diagnosis, surveillance and control, World Health Organization, pp: 1-122.
  8. Schneider MC, Najera P, Pereira MM, Machado G, dos Anjos CB, et al. (2015) Leptospirosis in Rio Grande do Sul, Brazil: An Ecosystem Approach in the Animal- Human Interface. PLoS Negl Trop Dis 9(11): e0004095.
  9. (2019) Health Surveillance Guide. In: 3rd (Edn.), Brazil, Ministry of Health, pp: 1-741.
  10. Genovez ME (2009) Leptospirosis: A Disease Occurring Beyond the Rainy Season! Biological 71(1): 1-3.
  11. Costa F, Hagan JE, Calcagno J, Kane M, Torgerson P, et al. (2015) Global Morbidity and Mortality of Leptospirosis: A Systematic Review. PLoS Negl Trop Dis 9(9): e0003898.
  12. Oliveira TV, Marinho DP, Costa NC, Kligerman DC (2009) Climate variables, living conditions and the health of the population: leptospirosis in the city of Rio de Janeiro from 1996 to 2009. Cien Saude Colet 17(6): 1569-1576.
  13. Pereira C (2014) Social cost of leptospirosis in Brazil and the effect of extreme rainfall in Nova Friburgo to increase the number of cases of the disease. Oswaldo Cruz Foundation.
  14. Lara JM, Zuben AV, Costa JV, Donalisio MR, Francisco PMSB (2019) Leptospirosis in Campinas, Sao Paulo, Brazil: 2007-2014. Rev Bras Epidemiol 22: e190016.
  15. Boey K, Shiokawa K, Rajeev S (2019) Leptospira infection in rats: A literature review of global prevalence  and  distribution.  PLoS  Negl  Trop  Dis 13(8): e0007499.
  16. Siguiura, Igor MS (2019) Leptospirose no estado do Paraná, Brasil: uma abordagem de saúde única. Rev Saúde Pública do Paraná 2(2): 77-84.
  17. Guerra  MA  (2009)  Leptospirosis.  J  Am  Vet  Med  Assoc 234(4): 472-478.
  18. McBride AJ, Athanazio DA, Reis MG, Ko AI (2005) Leptospirosis. Curr Opin Infect Dis 18(5): 376-386.
  19. Escócio C, Genovez ME, Castro V, Piatti RM, Gabriel FHL, et al. (2010) Influence Of Environmental Conditions On The Transmission Of Leptospirosis Between Sheep And Bovine Breeding In The Region Of Sorocaba, Sp. Arq Inst Biol 77(3): 371-379.
  20. Levett PN (2001) Leptospirosis. Clin Microbiol Rev 14(2): 296-326.
  21. Sampaio GP, Wanderley MR, Casseb GB, Negreiros MAMP (2011) Epidemiological description of leptospirosis cases in a tertiary hospital in Rio Branco. Rev Soc Bras Clin Med São Paulo 9(5): 338-342.
  22. Adler  B,  Peña  MA  (2010)  Leptospira  and  leptospiro- sis. Vet Microbiol 140(3-4): 287-296.
  23. Perolat P, Chappel RJ, Adler B, Baranton G, Bulach DM, et al. (1998) Leptospira fainei sp. nov., isolated from pigs in Australia. Int J Syst Bacteriol 3: 851-858.
  24. Fontaine GA, Aviat F, Thorin C (2015) Waterborne Leptospirosis: Survival and Preservation of the Virulence of Pathogenic Leptospira spp. in Fresh Water. Curr Microbiol 71(1): 136-142.
  25. Massana AC, Pedra GG, Wunder EA, Diggle PJ, Begon M, et al. (2018) Quantification of Leptospira interrogans Survival in Soil and Water Microcosms. Appl Environ Microbiol 84(13): e00507-18.
  26. Fouts DE, Matthias MA, Adhikarla H, Adler B, Santos LA, et al. (2016) What Makes a Bacterial Species Pathogenic?:Comparative Genomic Analysis of the Genus Leptospira. PLoS Negl Trop Dis 10(2): e0004403.
  27. Picardeau M (2017) Virulence of the zoonotic agent of leptospirosis: still terra incognita? Nat Rev Microbiol 15(5): 297-307.
  28. Vincent AT, Schiettekatte O, Goarant C, Neela VK, Bernet E, et al. (2019) Revisiting the taxonomy and evolution of pathogenicity of the genus Leptospira through the prism of genomics. PLoS Negl Trop Dis 13(5): e0007270.
  29. Vincent AT, Schiettekatte O, Goarant C, Neela VK, Bernet E, et al. (2019) Revisiting the taxonomy and evolution of pathogenicity of the genus Leptospira through the prism of genomics. PLoS Negl Trop Dis 13(5): e0007270.
  30. Thibeaux R, Iraola G, Ferrés I, Bierque E, Girault D, et al. (2018) Deciphering the unexplored Leptospira diversity from soils uncovers genomic evolution to virulence. Microb Genomics 4(1): e000144.
  31. Thibeaux R, Girault D, Bierque E, Soupé Gilbert ME, Rettinger A, et al. (2018) Biodiversity of Environmental Leptospira: Improving Identification and Revisiting the Diagnosis. Front Microbiol.
  32. Schneider AG, Massana AC, Hacker KP, Wunder EAJ, Begon M, et al. (2018) Quantification of pathogenic Leptospira in the soils of a Brazilian urban slum. PLoS Negl Trop Dis 12(4): e0006415.
  33. Barragan V, Olivas S, Keim P, Pearson T (2017) Critical Knowledge Gaps in Our Understanding of Environmental Cycling and Transmission of Leptospira spp. Appl Environ Microbiol 83(19): e01190-17.
  34. Matsunaga J, Lo M, Bulach DM, Zuerner RL, Adler B, et al. (2007) Response of Leptospira interrogans to Physiologic Osmolarity: Relevance in Signaling the Environment-to-Host Transition. Infect Immun 75(6): 2864-2874.
  35. Bierque E, Thibeaux R, Girault D, Soupé Gilbert ME, Goarant C (2020) A systematic review of Leptospira in water and soil environments. Plos One15(1): e0227055.
  36. Thibeaux R, Geroult S, Benezech C, Chabaud SP, Soupé Gilbert ME, et al. (2017) Seeking the environmental source of Leptospirosis reveals durable bacterial viability in river soils. Plos Neglected Trop Dis 11(2): e0005414.
  37. Riediger IN, Hoffmaster AR, Massana AC, Biondo AW, Ko AI, et al. (2016) An Optimized Method for Quantification of Pathogenic Leptospira in Environmental Water Samples. PLoS One 11(8): e0160523.
  38. Masuzawa T, Sakakibara K, Saito M, Hidaka Y, Villanueva SY, et al. (2018) Characterization of Leptospira species isolated from soil collected in Japan. Microbiol Immunol 62(1): 55-59.
  39. Scialfa E, Grune S, Brihuega B, Aguirre P, Rivero M (2018) Isolation of saprophytic Leptospira spp. from a selected environmental water source of Argentina. Rev Argent Microbiol 50(3): 323-326.
  40. Kim JS (1987) Leptospirosis: A Newly Identified Disease in Korea. Asia Pacific J Public Heal 1(1): 61-68.
  41. Henry RA, Johnson RC (1978) Distribution of the genus Leptospira in soil and water. Appl Environ Microbiol 35(3): 492-499.
  42. Mohd Ali MR, Mohamad Safiee AW, Yusof NY, Fauzi MH, Yean Yean C, et al. (2018) Isolation of Leptospira kmetyi from residential areas of patients with leptospirosis in Kelantan, Malaysia. J Infect Public Health 11(4): 578- 580.
  43. Hagan JE, Moraga P, Costa F, Capian N, Ribeiro GS, et al. (2016) Spatiotemporal Determinants of Urban Leptospirosis Transmission: Four-Year Prospective Cohort Study of Slum Residents in Brazil. Plos Neglected Trop Dis 10(1): e0004275.
  44. Schneider MC, Najera P, Aldighieri S, Bacallao J, Soto A, et al. (2012) Leptospirosis outbreaks in Nicaragua: identifying critical areas and exploring drivers for evidence-based planning. Int J Environ Res Public Health 9(11): 3883-3910.
  45. Neto JLS, Aleixo NCR (2010) Rainfall Events Extremes and Health: Perspectives of Interaction By Leptospirosis Cases in Urban Environment. Hygeia 6(11): 118-132.
  46. Rood EJJ, Goris MGA, Pijnacker R, Bakker MI, Hartskeerl RA (2017) Environmental risk of leptospirosis infections in the Netherlands: Spatial modelling of environmental risk factors of leptospirosis in the Netherlands. PLoS One 12(10): e0186987.
  47. Marchi MNA (2021) Spatial analysis of human cases of leptospirosis and leishmaniasis, an environmental approach. Universidade Estadual de Londrina.
  48. Gonçalves DD, Benitez A, Lopes Mori FMR, Alves LA, Freire RL, et al. (2013) Zoonoses in humans from small rural properties in Jataizinho, Parana, Brazil. Brazilian J Microbiol 44(1): 125-131.
  49. Schneider MC, Najera P, Pereira MM, Machado G, dos Anjos CB, et al. (2015) Leptospirosis in Rio Grande do Sul, Brazil: An Ecosystem Approach in the Animal- Human Interface. PLoS Negl Trop Dis 9(11): e0004095.
  50. Polo N, Machado G, Rodrigues R, Patricia N, Zanzi CM, et al. (2019) A One Health Approach to Investigating Leptospira Serogroups and Their Spatial Distributions among Humans and Animals in Rio Grande do Sul, Brazil, 2013-2015. Trop Med Infect Dis 4(1): 42.
  51. Galan DI, Roess AA, Pereira SVC, Schneider MC (2021) Epidemiology of human leptospirosis in urban and rural areas of Brazil, 2000-2015. PLoS One 16(3): e0247763.
  52. Bier D, Shimakura SE, Morikawa VM, Ullmann LS, Kikuti M, et al. (2013) Spatial analysis of the risk of canine leptospirosis in the Vila Pantanal, Curitiba, Paraná, Brazil. Pesqui Vet Bras 33(1): 74-79.
  53. Caldart ET, Constantino C, Sbruzzi Pasquali AK, Benitez AN, Hamada FN, et al. (2015) Zoonosis in dogs and cats attended by the Birth Control Project: Toxoplasma gondii, Leishmania spp. and Leptospira spp., serodiagnosis and epidemiology. Semin Agrar 36(1): 253-265.
  54. Benitez A, Rodrigues GG, Gonçalves DD, Burke JC, Alves LA, et al. (2010) Leptospirosis in stray dogs found in university campus: Serological evaluation and urine direct exam. Semin Agrar 31: 191-196.
  55. Benitez AN, Monica TC, Miura AC, Romanelli MS, Giordano LGP, et al. (2021) Spatial and Simultaneous Seroprevalence of Anti-Leptospira Antibodies in Owners and Their Domiciled Dogs in a Major City of Southern Brazil. Front Vet Sci.
  56. Miraglia F, de Morais ZM, Dellagostin OA, Seixas FK, Freitas JC, et al. (2013) Molecular and serological characterization of Leptospira interrogans serovar Canicola isolated from dogs, swine, and bovine in Brazil. Trop Anim Health Prod 45(1): 117-121.
  57. Zacarias FGS, Marques DRC, Cardoso MJL, Freitas JC, Zamarian TP, et al. (2015) Frequency of Anti-Leptospira Spp. In Dogs Care At The Veterinary Hospital Of The Universidade Estadual Do Norte Do Paraná-Uenp. Arq Ciências Veterinárias e Zool da UNIPAR. 17: 91-95.
  58. Chideroli RT, Pereira UP, Gonçalves DD, Nakamura AY, Alfieri AA, et al. (2016) Isolation and molecular characterization of Leptospira borgpetersenii serovar Hardjo strain Hardjobovis in the urine of naturally infected cattle in Brazil. Genet Mol Res 15(1).
  59. Delbem ÁCB, Freire RL, Silva CA da, Müller EE, Dias RA, et al. (2004) Risk factors associated to leptospirosis seropositiveness in sows. Ciência Rural 34(3): 847-852.
  60. Honório CV, Rodrigues FF, Laurence Zini LM, Nobre Simões AML (2012) Environmental and socioeconomic factors related to the distribution of leptospirosis cases in the state of Pernambuco, Brazil, 2001-2009. Cad Saúde Coletiva 20(1): 49-56.
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@article{marchi2022,
  title   = {Influence of Environmental Factors on Occurrence of
Leptospirosis in Humans and Animals in Brazil-A Review},
  author  = {Marchi MNA},
  journal = {Epidemiology International Journal},
  year    = {2022},
  volume  = {6},
  number  = {3},
  doi     = {10.23880/eij-16000241}
}
Marchi MNA (2022). Influence of Environmental Factors on Occurrence of
Leptospirosis in Humans and Animals in Brazil-A Review. Epidemiology International Journal, 6(3). https://doi.org/10.23880/eij-16000241
TY  - JOUR
TI  - Influence of Environmental Factors on Occurrence of
Leptospirosis in Humans and Animals in Brazil-A Review
AU  - Marchi MNA
JO  - Epidemiology International Journal
PY  - 2022
VL  - 6
IS  - 3
DO  - 10.23880/eij-16000241
ER  -